Skip to main content
PMC home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2000 Feb 29;355(1394):267–273. doi: 10.1098/rstb.2000.0563

Bilateral receptive field neurons and callosal connections in the somatosensory cortex.

Y Iwamura 1
PMCID: PMC1692728  PMID: 10724460

Abstract

Earlier studies recording single neuronal activity with bilateral receptive fields in the primary somatosensory cortex of monkeys and cats agreed that the bilateral receptive fields were related exclusively to the body midline and that the ipsilateral information reaches the cortex via callosal connections since they are dense in the cortical region representing the midline structures of the body while practically absent in the regions representing the distal extremities. We recently found a substantial number of neurons with bilateral receptive fields on hand digits, shoulders-arms or legs-feet in the caudalmost part (areas 2 and 5) of the postcentral gyrus in awake Japanese monkeys (Macaca fuscata). I review these results, discuss the functional implications of this bilateral representation in the postcentral somatosensory cortex from a behavioural standpoint and give a new interpretation to the midline fusion theory.

Full Text

The Full Text of this article is available as a PDF (142.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Akers R. M., Killackey H. P. Organization of corticocortical connections in the parietal cortex of the rat. J Comp Neurol. 1978 Oct 1;181(3):513–537. doi: 10.1002/cne.901810305. [DOI] [PubMed] [Google Scholar]
  2. Armstrong-James M., George M. J. Bilateral receptive fields of cells in rat Sm1 cortex. Exp Brain Res. 1988;70(1):155–165. doi: 10.1007/BF00271857. [DOI] [PubMed] [Google Scholar]
  3. Barbaresi P., Conti F., Manzoni T. Topography and receptive field organization of the body midline representation in the ventrobasal complex of the cat. Exp Brain Res. 1984;54(2):327–336. doi: 10.1007/BF00236234. [DOI] [PubMed] [Google Scholar]
  4. Berlucchi G., Gazzaniga M. S., Rizzolatti G. Microelectrode analysis of transfer of visual information by the corpus callosum. Arch Ital Biol. 1967 Nov;105(4):583–596. [PubMed] [Google Scholar]
  5. Berlucchi G., Rizzolatti G. Binocularly driven neurons in visual cortex of split-chiasm cats. Science. 1968 Jan 19;159(3812):308–310. doi: 10.1126/science.159.3812.308. [DOI] [PubMed] [Google Scholar]
  6. Burbaud P., Doegle C., Gross C., Bioulac B. A quantitative study of neuronal discharge in areas 5, 2, and 4 of the monkey during fast arm movements. J Neurophysiol. 1991 Aug;66(2):429–443. doi: 10.1152/jn.1991.66.2.429. [DOI] [PubMed] [Google Scholar]
  7. CHOUDHURY B. P., WHITTERIDGE D., WILSON M. E. THE FUNCTION OF THE CALLOSAL CONNECTIONS OF THE VISUAL CORTEX. Q J Exp Physiol Cogn Med Sci. 1965 Apr;50:214–219. doi: 10.1113/expphysiol.1965.sp001783. [DOI] [PubMed] [Google Scholar]
  8. Caminiti R., Sbriccoli A. The callosal system of the superior parietal lobule in the monkey. J Comp Neurol. 1985 Jul 1;237(1):85–99. doi: 10.1002/cne.902370107. [DOI] [PubMed] [Google Scholar]
  9. Clarey J. C., Tweedale R., Calford M. B. Interhemispheric modulation of somatosensory receptive fields: evidence for plasticity in primary somatosensory cortex. Cereb Cortex. 1996 Mar-Apr;6(2):196–206. doi: 10.1093/cercor/6.2.196. [DOI] [PubMed] [Google Scholar]
  10. Conti F., Fabri M., Manzoni T. Bilateral receptive fields and callosal connectivity of the body midline representation in the first somatosensory area of primates. Somatosens Res. 1986;3(4):273–289. doi: 10.3109/07367228609144588. [DOI] [PubMed] [Google Scholar]
  11. Dreyer D. A., Loe P. R., Metz C. B., Whitsel B. L. Representation of head and face in postcentral gyrus of the macaque. J Neurophysiol. 1975 May;38(3):714–733. doi: 10.1152/jn.1975.38.3.714. [DOI] [PubMed] [Google Scholar]
  12. Duffy F. H., Burchfiel J. L. Somatosensory system: organizational hierarchy from single units in monkey area 5. Science. 1971 Apr 16;172(3980):273–275. doi: 10.1126/science.172.3980.273. [DOI] [PubMed] [Google Scholar]
  13. EBNER F. F., MYERS R. E. Corpus callosum and the interhemispheric transmission of tactual learning. J Neurophysiol. 1962 May;25:380–391. doi: 10.1152/jn.1962.25.3.380. [DOI] [PubMed] [Google Scholar]
  14. Gould H. J., 3rd, Kaas J. H. The distribution of commissural terminations in somatosensory areas I and II of the grey squirrel. J Comp Neurol. 1981 Mar 1;196(3):489–504. doi: 10.1002/cne.901960311. [DOI] [PubMed] [Google Scholar]
  15. Hayama T., Ogawa H. Regional differences of callosal connections in the granular zones of the primary somatosensory cortex in rats. Brain Res Bull. 1997;43(3):341–347. doi: 10.1016/s0361-9230(97)00018-x. [DOI] [PubMed] [Google Scholar]
  16. Hubel D. H., Wiesel T. N. Cortical and callosal connections concerned with the vertical meridian of visual fields in the cat. J Neurophysiol. 1967 Nov;30(6):1561–1573. doi: 10.1152/jn.1967.30.6.1561. [DOI] [PubMed] [Google Scholar]
  17. Hunter M., Ettlinger G., Maccabe J. J. Intermanual transfer in the monkey as a function of amount of callosal sparing. Brain Res. 1975 Aug 8;93(2):223–240. doi: 10.1016/0006-8993(75)90347-9. [DOI] [PubMed] [Google Scholar]
  18. Innocenti G. M., Manzoni T., Spidalieri G. Patterns of the somesthetic messages transferred through the corpus callosum. Exp Brain Res. 1974 Mar 29;19(5):447–466. doi: 10.1007/BF00236110. [DOI] [PubMed] [Google Scholar]
  19. Iwamura Y. Hierarchical somatosensory processing. Curr Opin Neurobiol. 1998 Aug;8(4):522–528. doi: 10.1016/s0959-4388(98)80041-x. [DOI] [PubMed] [Google Scholar]
  20. Iwamura Y., Iriki A., Tanaka M. Bilateral hand representation in the postcentral somatosensory cortex. Nature. 1994 Jun 16;369(6481):554–556. doi: 10.1038/369554a0. [DOI] [PubMed] [Google Scholar]
  21. Iwamura Y., Tanaka M. Representation of reaching and grasping in the monkey postcentral gyrus. Neurosci Lett. 1996 Aug 23;214(2-3):147–150. doi: 10.1016/0304-3940(96)12911-6. [DOI] [PubMed] [Google Scholar]
  22. Iwamura Y., Tanaka M., Sakamoto M., Hikosaka O. Diversity in receptive field properties of vertical neuronal arrays in the crown of the postcentral gyrus of the conscious monkey. Exp Brain Res. 1985;58(2):400–411. doi: 10.1007/BF00235321. [DOI] [PubMed] [Google Scholar]
  23. Iwamura Y., Tanaka M., Sakamoto M., Hikosaka O. Rostrocaudal gradients in the neuronal receptive field complexity in the finger region of the alert monkey's postcentral gyrus. Exp Brain Res. 1993;92(3):360–368. doi: 10.1007/BF00229023. [DOI] [PubMed] [Google Scholar]
  24. Iwamura Y., Tanaka M., Sakamoto M., Hikosaka O. Vertical neuronal arrays in the postcentral gyrus signaling active touch: a receptive field study in the conscious monkey. Exp Brain Res. 1985;58(2):412–420. doi: 10.1007/BF00235322. [DOI] [PubMed] [Google Scholar]
  25. Jones E. G., Coulter J. D., Wise S. P. Commissural columns in the sensory-motor cortex of monkeys. J Comp Neurol. 1979 Nov 1;188(1):113–135. doi: 10.1002/cne.901880110. [DOI] [PubMed] [Google Scholar]
  26. Jones E. G., Hendry S. H. Distribution of callosal fibers around the hand representations in monkey somatic sensory cortex. Neurosci Lett. 1980 Sep;19(2):167–172. doi: 10.1016/0304-3940(80)90189-5. [DOI] [PubMed] [Google Scholar]
  27. Jones E. G., Powell T. P. Connexions of the somatic sensory cortex of the rhesus monkey. 3. Thalamic connexions. Brain. 1970;93(1):37–56. doi: 10.1093/brain/93.1.37. [DOI] [PubMed] [Google Scholar]
  28. Jones E. G., Powell T. P. Connexions of the somatic sensory cortex of the rhesus monkey. II. Contralateral cortical connexions. Brain. 1969;92(4):717–730. doi: 10.1093/brain/92.4.717. [DOI] [PubMed] [Google Scholar]
  29. Jones E. G., Powell T. P. The commissural connexions of the somatic sensory cortex in the cat. J Anat. 1968 Nov;103(Pt 3):433–455. [PMC free article] [PubMed] [Google Scholar]
  30. Jones E. G., Schwark H. D., Callahan P. A. Extent of the ipsilateral representation in the ventral posterior medial nucleus of the monkey thalamus. Exp Brain Res. 1986;63(2):310–320. doi: 10.1007/BF00236848. [DOI] [PubMed] [Google Scholar]
  31. Karol E. A., Pandya D. N. The distribution of the corpus callosum in the Rhesus monkey. Brain. 1971;94(3):471–486. doi: 10.1093/brain/94.3.471. [DOI] [PubMed] [Google Scholar]
  32. Killackey H. P., Gould H. J., 3rd, Cusick C. G., Pons T. P., Kaas J. H. The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys. J Comp Neurol. 1983 Oct 1;219(4):384–419. doi: 10.1002/cne.902190403. [DOI] [PubMed] [Google Scholar]
  33. Leinonen L., Hyvärinen J., Nyman G., Linnankoski I. I. Functional properties of neurons in lateral part of associative area 7 in awake monkeys. Exp Brain Res. 1979 Jan 15;34(2):299–320. doi: 10.1007/BF00235675. [DOI] [PubMed] [Google Scholar]
  34. Manzoni T., Barbaresi P., Bellardinelli E., Caminiti R. Callosal projections from the two body midlines. Exp Brain Res. 1980;39(1):1–9. doi: 10.1007/BF00237063. [DOI] [PubMed] [Google Scholar]
  35. Manzoni T., Barbaresi P., Conti F., Fabri M. The callosal connections of the primary somatosensory cortex and the neural bases of midline fusion. Exp Brain Res. 1989;76(2):251–266. doi: 10.1007/BF00247886. [DOI] [PubMed] [Google Scholar]
  36. Mountcastle V. B., Lynch J. C., Georgopoulos A., Sakata H., Acuna C. Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol. 1975 Jul;38(4):871–908. doi: 10.1152/jn.1975.38.4.871. [DOI] [PubMed] [Google Scholar]
  37. Ogawa H., Ito S., Nomura T. Oral cavity representation at the frontal operculum of macaque monkeys. Neurosci Res. 1989 Apr;6(4):283–298. doi: 10.1016/0168-0102(89)90021-7. [DOI] [PubMed] [Google Scholar]
  38. Pandya D. N., Seltzer B. Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. J Comp Neurol. 1982 Jan 10;204(2):196–210. doi: 10.1002/cne.902040208. [DOI] [PubMed] [Google Scholar]
  39. Pandya D. N., Vignolo L. A. Interhemispheric projections of the parietal lobe in the rhesus monkey. Brain Res. 1969 Sep;15(1):49–65. doi: 10.1016/0006-8993(69)90309-6. [DOI] [PubMed] [Google Scholar]
  40. Pidoux B., Verley R. Projections on the cortical somatic I barrel subfield from ipsilateral vibrissae in adult rodents. Electroencephalogr Clin Neurophysiol. 1979 Jun;46(6):715–726. doi: 10.1016/0013-4694(79)90111-1. [DOI] [PubMed] [Google Scholar]
  41. Pons T. P., Kaas J. H. Connections of area 2 of somatosensory cortex with the anterior pulvinar and subdivisions of the ventroposterior complex in macaque monkeys. J Comp Neurol. 1985 Oct 1;240(1):16–36. doi: 10.1002/cne.902400103. [DOI] [PubMed] [Google Scholar]
  42. Rausell E., Jones E. G. Histochemical and immunocytochemical compartments of the thalamic VPM nucleus in monkeys and their relationship to the representational map. J Neurosci. 1991 Jan;11(1):210–225. doi: 10.1523/JNEUROSCI.11-01-00210.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Ridley R. M., Ettlinger G. Further evidence of impaired tactile learning after removals of the second somatic sensory projection cortex (SII) in the monkey. Exp Brain Res. 1978 Apr 14;31(4):475–488. doi: 10.1007/BF00239806. [DOI] [PubMed] [Google Scholar]
  44. Sakata H., Takaoka Y., Kawarasaki A., Shibutani H. Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey. Brain Res. 1973 Dec 21;64:85–102. doi: 10.1016/0006-8993(73)90172-8. [DOI] [PubMed] [Google Scholar]
  45. Schwarz D. W., Fredrickson J. M. Tactile direction sensitivity of area 2 oral neurons in the rhesus monkey cortex. Brain Res. 1971 Apr 2;27(2):397–401. doi: 10.1016/0006-8993(71)90270-8. [DOI] [PubMed] [Google Scholar]
  46. Seltzer B., Pandya D. N. Posterior parietal projections to the intraparietal sulcus of the rhesus monkey. Exp Brain Res. 1986;62(3):459–469. doi: 10.1007/BF00236024. [DOI] [PubMed] [Google Scholar]
  47. Shanks M. F., Pearson R. C., Powell T. P. The callosal connexions of the primary somatic sensory cortex in the monkey. Brain Res. 1985 Apr;356(1):43–65. doi: 10.1016/0165-0173(85)90018-9. [DOI] [PubMed] [Google Scholar]
  48. Shanks M. F., Powell T. P. An electron microscopic study of the termination of thalamocortical fibres in areas 3b, 1 and 2 of the somatic sensory cortex in the monkey. Brain Res. 1981 Aug 10;218(1-2):35–47. doi: 10.1016/0006-8993(81)90987-2. [DOI] [PubMed] [Google Scholar]
  49. Shanks M. F., Rockel A. J., Powell T. P. The commissural fibre connections of the primary somatic sensory cortex. Brain Res. 1975 Nov 7;98(1):166–171. doi: 10.1016/0006-8993(75)90516-8. [DOI] [PubMed] [Google Scholar]
  50. Shin H. C., Won C. K., Jung S. C., Oh S., Park S., Sohn J. H. Interhemispheric modulation of sensory transmission in the primary somatosensory cortex of rats. Neurosci Lett. 1997 Jul 18;230(2):137–139. doi: 10.1016/s0304-3940(97)00486-2. [DOI] [PubMed] [Google Scholar]
  51. Taoka M., Toda T., Iwamura Y. Representation of the midline trunk, bilateral arms, and shoulders in the monkey postcentral somatosensory cortex. Exp Brain Res. 1998 Dec;123(3):315–322. doi: 10.1007/s002210050574. [DOI] [PubMed] [Google Scholar]
  52. Whitsel B. L., Petrucelli L. M., Werner G. Symmetry and connectivity in the map of the body surface in somatosensory area II of primates. J Neurophysiol. 1969 Mar;32(2):170–183. doi: 10.1152/jn.1969.32.2.170. [DOI] [PubMed] [Google Scholar]
  53. Zeki S. M. Functional specialisation in the visual cortex of the rhesus monkey. Nature. 1978 Aug 3;274(5670):423–428. doi: 10.1038/274423a0. [DOI] [PubMed] [Google Scholar]

Articles from Philosophical Transactions of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES